Exploring the miRNA Regulatory Network Using Evolutionary Correlations

PLoS Computational Biology

Volumn 10, Issue 10, 2014, Pages

  Obermayer, Benedikt ^a,b   Levine, Erel ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COORDINATION REACTIONS; GENES; PHYLOGENETIC; PROTEINS; RNA;

BAYESIAN FRAMEWORKS; BINDING-SITES; COLLECTIVE EFFECTS; MRNA LEVELS; NETWORK LINKS; POST-TRANSCRIPTIONAL REGULATIONS; PROTEIN LEVEL; REGULATORY NETWORK; TARGET SITES; WHOLE GENOME ALIGNMENT;

BINDING SITES;

MICRORNA;

3' UNTRANSLATED REGION; ARTICLE; BAYES THEOREM; CONTROLLED STUDY; EVOLUTIONARY CORRELATION; GENE CONTROL; GENE LOCUS; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC ASSOCIATION; GENETIC CONSERVATION; HUMAN; MATHEMATICAL ANALYSIS; MOLECULAR MODEL; NONHUMAN; PHYLOGENETIC TREE; RNA ANALYSIS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; VERTEBRATE; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PHYLOGENY; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; HUMANS; MICE; MICRORNAS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; ZEBRAFISH;

EID: 84908311508     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003860     Document Type: Article

References (83)

1. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215–233.
2. Chen K, Rajewsky N, (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8: 93–103.
3. Small EM, Olson EN, (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469: 336.
4. Pauli A, Rinn JL, Schier AF, (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12: 136–149.
5. Esteller M, (2011) Non-coding RNAs in human disease. Nat Rev Genet 12: 861–874.
6. Liu N, Okamura K, Tyler DM, Phillips MD, Chung WJ, et al. (2008) The evolution and functional diversification of animal microRNA genes. Cell Res 18: 985–996.
7. Hertel J, Lindemeyer M, Missal K, Fried C, Tanzer A, et al. (2006) The expansion of the metazoan microRNA repertoire. BMC Genomics 7: 25.
8. Carthew RW, Sontheimer EJ, (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136: 642–655.
9. Grimson A, Farh KKH, Johnston WK, Garrett-Engele P, Lim LP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91–105.
10. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, et al. (2008) The impact of microRNAs on protein output. Nature 455: 64–71.
11. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, et al. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58–63.
12. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, et al. (2010) Transcriptome-wide Identification of RNA-Binding Protein and microRNA Target Sites by PAR-CLIP. Cell 141: 129–141.
13. Chi SW, Zang JB, Mele A, Darnell RB, (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479–486.
14. Leung AK, Young AG, Bhutkar A, Zheng GX, Bosson AD, et al. (2011) Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat Struct Mol Biol 18: 237–244.
15. Khorshid M, Hausser J, Zavolan M, van Nimwegen E, (2013) A biophysical miRNA-mRNA interaction model infers canonical and noncanonical targets. Nat Methods 10: 253–255.
16. Majoros WH, Lekprasert P, Mukherjee N, Skalsky RL, Corcoran DL, et al. (2013) MicroRNA target site identification by integrating sequence and binding information. Nat Methods 10: 630–633.
17. Helwak A, Kudla G, Dudnakova T, Tollervey D, (2013) Mapping the Human miRNA Interactome by Clash Reveals Frequent Noncanonical Binding. Cell 153: 654–665.
18. Grosswendt S, Filipchyk A, Manzano M, Klironomos F, Schilling M, et al. (2014) Unambiguous Identification of miRNA:Target Site Interactions by Different Types of Ligation Reactions. Mol Cell 54: 1042–1054.
19. Farh KKH, Grimson A, Jan C, Lewis BP, Johnston WK, et al. (2005) The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310: 1817–1821.
20. Huntzinger E, Izaurralde E, (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99.
21. Lee R, Feinbaum R, Ambros V, (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843–854.
22. Reinhart B, Slack F, Basson M, Pasquinelli A, Bettinger J, et al. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901–906.
23. Flynt AS, Lai EC, (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet 9: 831–842.
24. Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, et al. (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3: e215.
25. Alvarez-Saavedra E, Horvitz HR, (2010) Many families of C. elegans microRNAs are not essential for development or viability. Curr Biol 20: 367–373.
26. Valastyan S, Benaich N, Chang A, Reinhardt F, Weinberg RA, (2009) Concomitant suppression of three target genes can explain the impact of a microRNA on metastasis. Genes Dev 23: 2592–2597.
27. Seitz H, (2009) Redefining microRNA targets. Curr Biol 19: 870–873.
28. Jost D, Nowojewski A, Levine E, (2013) Regulating the many to benefit the few: role of weak small RNA targets. Biophys J 104: 1773–1782.
29. Ebert MS, Sharp PA, (2012) Roles for MicroRNAs in Conferring Robustness to Biological Processes. Cell 149: 515–524.
30. Enright AJ, John B, Gaul U, Tuschl T, Sander C, et al. (2003) MicroRNA targets in Drosophila. Genome Biol 5: R1.
31. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15–20.
32. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, et al. (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495–500.
33. Ebert MS, Sharp PA, (2010) Emerging roles for natural microRNA sponges. Curr Biol 20: 858–61.
34. Sumazin P, Yang X, Chiu HS, Chung WJ, Iyer A, et al. (2011) An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 147: 370–381.
35. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, et al. (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147: 358–369.
36. Sass S, Dietmann S, Burk U, Brabletz S, Lutter D, et al. (2011) MicroRNAs coordinately regulate protein complexes. BMC Systems Biology 5: 136.
37. Tsang JS, Ebert MS, van Oudenaarden A, (2010) Genome-wide Dissection of MicroRNA Functions and Cotargeting Networks Using Gene Set Signatures. Mol Cell 38: 140–153.
38. Doniger SW, Fay JC, (2007) Frequent gain and loss of functional transcription factor binding sites. PLoS Comput Biol 3: e99.
39. Bradley RK, Li XY, Trapnell C, Davidson S, Pachter L, et al. (2010) Binding Site Turnover Produces Pervasive Quantitative Changes in Transcription Factor Binding between Closely Related Drosophila Species. PLoS Biol 8: e1000343.
40. Schmidt D, Wilson M, Ballester B, Schwalie P, Brown G, et al. (2010) Five-Vertebrate ChIp-seq Reveals the Evolutionary Dynamics of Transcription Factor Binding. Science 328: 1036–1040.
41. Stefflova K, Thybert D, Wilson MD, Streeter I, Aleksic J, et al. (2013) Cooperativity and Rapid Evolution of Cobound Transcription Factors in Closely Related Mammals. Cell 154: 530–540.
42. Davidson EH (2001) Genomic Regulatory Systems: Development and Evolution. San Diego, Ca, U.S.A.: Elsevier Academic Press.
43. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, et al. (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20: 1377–1419.
44. Wilson MD, Odom DT, (2009) Evolution of transcriptional control in mammals. Curr Opin Genet Dev 19: 579–585.
45. Fay J, Wittkopp PJ, (2008) Evaluating the role of natural selection in the evolution of gene regulation. Heredity 100: 191–199.
46. Lynch M, (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. P Natl Acad Sci USA 104 Suppl 1: 8597–8604.
47. Richard W, Lusk MBE (2010) Evolutionary Mirages: Selection on Binding Site Composition Creates the Illusion of Conserved Grammars in Drosophila Enhancers. PLoS Genetics 6.
48. Grün D, Wang YL, Langenberger D, Gunsalus KC, Rajewsky N, (2005) microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput Biol 1: e13.
49. Eddy S, Durbin R, (1994) RNA sequence analysis using covariance models. Nucleic Acids Res 22: 2079–2088.
50. Neher E, (1994) How frequent are correlated changes in families of protein sequences? P Natl Acad Sci USA 91: 98–102.
51. Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, et al. (2011) Protein 3D Structure Computed from Evolutionary Sequence Variation. PLoS ONE 6: e28766.
52. Morcos F, Pagnani A, Marks DS, Sander C, Zecchina R, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. P Natl Acad Sci USA 108: 1293–301.
53. Tabach Y, Billi AC, Hayes GD, Newman MA, Zuk O, et al. (2012) Identification of small RNA pathway genes using patterns of phylogenetic conservation and divergence. Nature 493: 694–698.
54. Pellegrini M, Marcotte E, Thompson M, Eisenberg D, Yeates TO, (1999) Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. P Natl Acad Sci USA 96: 4285–4288.
55. Kheradpour P, Stark A, Roy S, Kellis M, (2007) Reliable prediction of regulator targets using 12 Drosophila genomes. Genome Res 17: 1919–1931.
56. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, et al. (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17: 1850–1864.
57. Friedman RC, Farh KKH, Burge CB, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92–105.
58. Gaidatzis D, van Nimwegen E, Hausser J, Zavolan M, (2007) Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 8: 69.
59. Lewis BP, Shih Ih, Jones-Rhoades MW, Bartel DP, Burge CB, (2003) Prediction of mammalian microRNA targets. Cell 115: 787–798.
60. Wainwright MJ, Jordan MI, (2007) Graphical Models, Exponential Families, and Variational Inference. FNT in Machine Learning 1: 1–305.
61. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, et al. (2007) A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing. Cell 129: 1401–1414.
62. Saetrom P, Heale BS, Snove O, Aagaard L, Alluin J, et al. (2007) Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic Acids Res 35: 2333–2342.
63. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, et al. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769–773.
64. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, van Dongen S, et al. (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312: 75–79.
65. Denzler R, Agarwal V, Stefano J, Bartel DP, Stoffel M, (2014) Assessing the ceRNA Hypothesis with Quantitative Measurements of miRNA and Target Abundance. Mol Cell 54: 1–11.
66. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, et al. (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495: 333–338.
67. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, et al. (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495: 384–388.
68. Leuthäusser I, (1986) An Exact Correspondence Between Eigen Evolution Model And A Two-Dimensional Ising System. J Chem Phys 84: 1884–1885.
69. Shekhar K, Ruberman CF, Ferguson AL, Barton JP, Kardar M, et al. (2013) Spin models inferred from patient-derived viral sequence data faithfully describe HIV fitness landscapes. Phys Rev E 88: 062705.
70. Sella G, Hirsh A, (2005) The application of statistical physics to evolutionary biology. P Natl Acad Sci USA 102: 9541–9546.
71. Mustonen V, Lässig M, (2005) Evolutionary population genetics of promoters: predicting binding sites and functional phylogenies. P Natl Acad Sci USA 102: 15936–15941.
72. Lässig M, (2007) From biophysics to evolutionary genetics: statistical aspects of gene regulation. BMC Bioinformatics 8 Suppl 6: S7.
73. Kimura M, (1962) On the probability of fixation of mutant genes in a population. Genetics 47: 713–719.
74. Genome 10K Community of Scientists (2009) Genome 10K: a proposal to obtain whole-genome sequence for 10,000 vertebrate species. J Hered 100: 659–674.
75. Kim H, Kuwano Y, Srikantan S, Lee E, Martindale J, et al. (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev 23: 1743–1748.
76. Kedde M, Strasser MJ, Boldajipour B, Vrielink JAO, Slanchev K, et al. (2007) RNA-Binding Protein Dnd1 Inhibits MicroRNA Access to Target mRNA. Cell 131: 1273–1286.
77. Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, et al. (2010) A Pumilio-induced RNA structure switch in p27-3′UTR controls miR-221 and miR-222 accessibility. Nature Cell Biology 12: 1014–1020.
78. Tsang J, Zhu J, van Oudenaarden A, (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26: 753–767.
79. Osella M, Bosia C, Corá D, Caselle M, (2011) The Role of Incoherent microRNA-Mediated Feedforward Loops in Noise Buffering. PLoS Comput Biol 7: e1001101.
80. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, et al. (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15: 1451–1455.
81. Blankenberg D, Taylor J, Nekrutenko A, Team G, (2011) Making whole genome multiple alignments usable for biologists. Bioinformatics 27: 2426–2428.
82. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ, (2006) miRbase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: 140–4.
83. Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, et al. (2013) A compendium of RNA-binding motifs for decoding gene regulation. Nature 499: 172–177.